Simian rhesus rotavirus is a unique heterologous (non-lapine) rotavirus strain capable of productive replication and horizontal transmission in rabbits Free

Abstract

Simian rhesus rotavirus (RRV) is the only identified heterologous (non-lapine) rotavirus strain capable of productive replication at a high inoculum dose of virus (>10 p.f.u.) in rabbits. To evaluate whether lower doses of RRV would productively infect rabbits and to obtain an estimate of the 50% infectious dose, rotavirus antibody-free rabbits were inoculated orally with RRV at inoculum doses of 10, 10 or 10 p.f.u. Based on faecal virus antigen or infectious virus shedding, RRV replication was observed with inoculum doses of 10 and 10 p.f.u., but not 10 p.f.u. Horizontal transmission of RRV to one of three mock-inoculated rabbits occurred 4–5 days after onset of virus antigen shedding in RRV-infected rabbits. Rabbits infected at 10 and 10, but not 10, p.f.u. of RRV developed rotavirus-specific immune responses and were completely (100%) protected from lapine ALA rotavirus challenge. These data confirm that RRV can replicate productively and spread horizontally in rabbits. In attempts to elucidate the genetic basis of the unusual replication efficacy of RRV in rabbits, the sequence of the gene encoding the lapine non-structural protein NSP1 was determined. Sequence analysis of the NSP1 of three lapine rotaviruses revealed a high degree of amino acid identity (85–88%) with RRV. Since RRV and lapine strains also share similar VP7s (96–97%) and VP4s (69–70%), RRV might replicate efficiently in rabbits because of the high relatedness of these three gene products, each implicated in host range restriction.

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2000-05-01
2024-03-29
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References

  1. Bridger, J. C., Woode, G. N., Jones, J., Flewett, T. H., Bryden, A. & Davies, H. (1975). Transmission of human rotaviruses to gnotobiotic piglets.Journal of Medical Microbiology 8, 565-569.[CrossRef] [Google Scholar]
  2. Bridger, J. C., Dhaliwal, W., Adamson, M. J. & Howard, C. R. (1998). Determinants of rotavirus host range restriction – a heterologous bovine NSP1 gene does not affect replication kinetics in the pig.Virology 245, 47-52.[CrossRef] [Google Scholar]
  3. Broome, R. L., Vo, P. T., Ward, R. L., Clark, H. F. & Greenberg, H. B. (1993). Murine rotavirus genes encoding outer capsid proteins VP4 and VP7 are not major determinants of host range restriction and virulence.Journal of Virology 67, 2448-2455. [Google Scholar]
  4. Burke, B. & Desselberger, U. (1996). Rotavirus pathogenicity.Virology 218, 299-305.[CrossRef] [Google Scholar]
  5. Burns, J. W., Krishnaney, A., Vo, P. T., Rouse, R., Anderson, L. & Greenberg, H. B. (1995). Analyses of homologous rotavirus infection in the mouse model.Virology 207, 143-153.[CrossRef] [Google Scholar]
  6. Ciarlet, M. & Liprandi, F. (1994). Serological and genomic characterization of two porcine rotaviruses with serotype G1 specificity.Journal of Clinical Microbiology 32, 269-272. [Google Scholar]
  7. Ciarlet, M., Hidalgo, M., Gorziglia, M. & Liprandi, F. (1994). Characterization of neutralization epitopes on the VP7 surface protein of serotype G11 porcine rotaviruses.Journal of General Virology 75, 1867-1873.[CrossRef] [Google Scholar]
  8. Ciarlet, M., Estes, M. K. & Conner, M. E. (1997). Comparative amino acid sequence analysis of the outer capsid protein VP4 from four lapine rotavirus strains reveals identity with genotype P[14] human rotavirus.Archives of Virology 142, 1059-1069.[CrossRef] [Google Scholar]
  9. Ciarlet, M., Estes, M. K., Barone, C., Ramig, R. F. & Conner, M. E. (1998a). Analysis of host range restriction determinants in the rabbit model: comparison of homologous and heterologous rotavirus infections.Journal of Virology 72, 2341-2351. [Google Scholar]
  10. Ciarlet, M., Crawford, S. E., Barone, C., Bertolotti-Ciarlet, A., Estes, M. K. & Conner, M. E. (1998b). Subunit rotavirus vaccine administered parenterally to rabbits induces active protective immunity.Journal of Virology 72, 9233-9246. [Google Scholar]
  11. Ciarlet, M., Gilger, M. A., Barone, C., McArthur, M., Estes, M. K. & Conner, M. E. (1998c). Rotavirus disease, but not infection and development of intestinal histopathological lesions, is age restricted in rabbits.Virology 251, 343-360.[CrossRef] [Google Scholar]
  12. Ciarlet, M., Liprandi, F., Conner, M. E. & Estes, M. K. (2000). Species specificity and interspecies relatedness in NSP4 genetic groups by comparative NSP4 sequence analyses of animal rotaviruses. Archives of Virology 145, 371–383.[CrossRef] [Google Scholar]
  13. Conner, M. E. & Ramig, R. F. (1996). Enteric diseases. In Viral Pathogenesis, pp. 713-743. Edited by N. Nathanson, R. Ahmed, F. González-Scarano, D. E. Griffin, K. V. Homes, F. A. Murphy & H. L. Robinson. New York: Lippincott-Raven.
  14. Conner, M. E., Estes, M. K. & Graham, D. Y. (1988). Rabbit model of rotavirus infection.Journal of Virology 62, 1625-1633. [Google Scholar]
  15. Conner, M. E., Gilger, M. A., Estes, M. K. & Graham, D. Y. (1991). Serologic and mucosal immune response to rotavirus infection in the rabbit model.Journal of Virology 65, 2562-2571. [Google Scholar]
  16. Conner, M. E., Crawford, S. E., Barone, C. & Estes, M. K. (1993). Rotavirus vaccine administered parenterally induces protective immunity.Journal of Virology 67, 6633-6641. [Google Scholar]
  17. Conner, M. E., Graham, D. Y. & Estes, M. K. (1997). Determination of the duration of a primary immune response and the ID50 of ALA rabbit rotavirus in rabbits.Archives of Virology 142, 2281-2294.[CrossRef] [Google Scholar]
  18. Crawford, S. E., Estes, M. K., Ciarlet, M., Barone, C., O’Neal, C., Cohen, J. & Conner, M. E. (1999). Heterotypic protection and induction of a broad heterotypic neutralization response by rotavirus-like particles.Journal of Virology 73, 4813-4822. [Google Scholar]
  19. Dunn, S. J., Cross, T. L. & Greenberg, H. B. (1994a). Comparison of the rotavirus nonstructural protein NSP1 (NS53) from different species by sequence analysis and northern blot hybridization.Virology 203, 178-183.[CrossRef] [Google Scholar]
  20. Dunn, S. J., Burns, J. W., Cross, T., Vo, P., Ward, R., Bremont, M. & Greenberg, H. B. (1994b). Comparison of VP4 and VP7 of five murine rotavirus strains.Virology 203, 250-259.[CrossRef] [Google Scholar]
  21. Feng, N., Burns, J. W., Bracey, L. & Greenberg, H. B. (1994). Comparisons of the mucosal and systemic humoral immune responses and subsequent protection in mice orally inoculated with homologous or heterologous rotaviruses.Journal of Virology 68, 7766-7773. [Google Scholar]
  22. Franco, M. A., Feng, N. & Greenberg, H. B. (1996). Molecular determinants of immunity and pathogenicity of rotavirus infection in the mouse model.Journal of Infectious Diseases 174, 47-50.[CrossRef] [Google Scholar]
  23. Fujiwara, Y. & Nakagomi, O. (1997). Interspecies sharing of two distinct nonstructural protein 1 alleles among human and animal rotaviruses as revealed by dot blot hybridization.Journal of Clinical Microbiology 35, 2703-2705. [Google Scholar]
  24. Gombold, J. L. & Ramig, R. F. (1986). Analysis of reassortment of genome segments in mice mixedly infected with rotavirus SA11 and RRV.Journal of Virology 57, 110-116. [Google Scholar]
  25. Gorziglia, M., Aguirre, Y., Hoshino, Y., Esparza, J., Blumentals, I., Askaa, J., Thompson, M., Glass, R. I., Kapikian, A. Z. & Chanock, R. M. (1986). VP7 serotype-specific glycoprotein of OSU porcine rotavirus: coding assignment and gene sequence.Journal of General Virology 67, 2445-2454.[CrossRef] [Google Scholar]
  26. Greenberg, H. B., Valdesuso, J., van Wyke, K., Midthun, K., Walsh, M., McAuliffe, V., Wyatt, R., Kalica, A., Flores, J. & Hoshino, Y. (1983). Production and preliminary characterization of monoclonal antibodies directed at two surface proteins of rhesus rotavirus.Journal of Virology 47, 267-275. [Google Scholar]
  27. Horie, Y., Masamune, O. & Nakagomi, O. (1997). Three major alleles of rotavirus NSP4 proteins identified by sequence analysis.Journal of General Virology 78, 2341-2346. [Google Scholar]
  28. Hoshino, Y., Saif, L. J., Kang, S.-Y., Sereno, M. M., Chen, W.-K. & Kapikian, A. Z. (1995). Identification of group A rotavirus genes associated with virulence of a porcine rotavirus and host range restriction of a human rotavirus in the gnotobiotic piglet model.Virology 209, 274-280.[CrossRef] [Google Scholar]
  29. Hua, J., Mansell, E. A. & Patton, J. T. (1993). Comparative analysis of the NS53 gene: conservation of the basic and cysteine-rich regions in the protein and possible stem–loop structures in the RNA.Virology 196, 372-378.[CrossRef] [Google Scholar]
  30. Hua, J., Chen, X. & Patton, J. T. (1994). Deletion mapping of the rotavirus metalloprotein NS53 (NSP1): the conserved cysteine-rich region is essential for virus-specific RNA binding.Journal of Virology 68, 3990-4000. [Google Scholar]
  31. Iša, P., Wood, A. R., Netherwood, T., Ciarlet, M., Imagawa, H. & Snodgrass, D. R. (1996). Survey of equine rotaviruses shows conservation of one P genotype in background of two G genotypes.Archives of Virology 141, 1601-1612.[CrossRef] [Google Scholar]
  32. Kirkwood, C. D. & Palombo, E. A. (1997). Genetic characterization of the rotavirus nonstructural protein, NSP4.Virology 236, 258-265.[CrossRef] [Google Scholar]
  33. Kojima, K., Taniguchi, K. & Kobayashi, N. (1996). Species-specific and interspecies relatedness of NSP1 sequences in human, porcine, bovine, feline, and equine rotavirus strains.Archives of Virology 141, 1-12.[CrossRef] [Google Scholar]
  34. McNeal, M. M., Broome, R. L. & Ward, R. L. (1994). Active immunity against rotavirus infection in mice is correlated with viral replication and titers of serum rotavirus IgA following vaccination.Virology 204, 642-650.[CrossRef] [Google Scholar]
  35. Mitchell, D. B. & Both, G. W. (1990). Conservation of a potential metal binding motif despite extensive sequence diversity in the rotavirus nonstructural protein NS53.Virology 174, 618-621.[CrossRef] [Google Scholar]
  36. Nakagomi, O. & Kaga, E. (1995). Distinctness of NSP1 gene of human rotavirus AU-1 from NSP1 gene of other human genogroups.Research in Virology 146, 423-428.[CrossRef] [Google Scholar]
  37. Nakagomi, O. & Nakagomi, T. (1996). Molecular epidemiology of human rotaviruses: genogrouping by RNA–RNA hybridization.Archives of Virology Supplementum 12, 93-98. [Google Scholar]
  38. O’Neal, C. M., Crawford, S. E., Estes, M. K. & Conner, M. E. (1997). Rotavirus VLPs administered mucosally induce protective immunity.Journal of Virology 71, 8707-8717. [Google Scholar]
  39. O’Neal, C. M., Clements, J. D., Estes, M. K. & Conner, M. E. (1998). Rotavirus 2/6-VLPs administered intranasally with cholera toxin, E. coli heat labile toxin and LT-R192G induce protection from rotavirus challenge.Journal of Virology 72, 3390-3393. [Google Scholar]
  40. Palombo, E. A. & Bishop, R. F. (1994). Genetic analysis of NSP1 genes of human rotaviruses isolated from neonates with asymptomatic infection.Journal of General Virology 75, 3635-3639.[CrossRef] [Google Scholar]
  41. Ramig, R. F. (1988). The effects of host age, virus dose, and virus strain on heterologous rotavirus infection of suckling mice.Microbial Pathogenesis 4, 189-202.[CrossRef] [Google Scholar]
  42. Stucker, G., Oshino, L. & Schmidt, N. J. (1980). Antigenic comparisons of two new rotaviruses from rhesus monkeys.Journal of Clinical Microbiology 11, 202-203. [Google Scholar]
  43. Thouless, M. E., DiGiacomo, R., Deeb, B. J. & Howard, H. J. (1988). Pathogenicity of rotavirus in rabbits.Journal of Clinical Microbiology 26, 943-947. [Google Scholar]
  44. Ward, R. L., McNeal, M. & Sheridan, J. (1990). Development of an adult mouse model for studies on protection against rotavirus.Journal of Virology 64, 5070-5075. [Google Scholar]
  45. Ward, R. L., McNeal, M. & Sheridan, J. (1992). Evidence that active protection following oral immunization of mice with live rotavirus is not dependent on neutralizing antibody.Virology 188, 57-66.[CrossRef] [Google Scholar]
  46. Ward, L. A., Yuan, L., Rosen, B. I., To, T. & Saif, L. J. (1996). Development of mucosal and systemic lymphoproliferative responses and protective immunity to human group A rotaviruses in a gnotobiotic pig model.Clinical and Diagnostic Laboratory Immunology 3, 342-350. [Google Scholar]
  47. Wu, H., Taniguchi, K., Urasawa, T. & Urasawa, S. (1993). Genomic relatedness of five equine rotavirus strains with different G serotype and P type specificities.Research in Virology 144, 455-464.[CrossRef] [Google Scholar]
  48. Xu, L., Tian, Y., Tarlow, O., Harbour, D. & McCrae, M. A. (1994). Molecular biology of rotaviruses. IX. Conservation and divergence in genome segment 5.Journal of General Virology 75, 3413-3421.[CrossRef] [Google Scholar]
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